Do Cryptic Reservoirs Threaten Gambiense-Sleeping Sickness Elimination?
2018; Elsevier BV; Volume: 34; Issue: 3 Linguagem: Inglês
10.1016/j.pt.2017.11.008
ISSN1471-5007
AutoresPhilippe Büscher, Jean-Mathieu Bart, Marleen Boelaert, Bruno Bucheton, Giuliano Cecchi, Nakul Chitnis, David Courtin, Luísa M. Figueiredo, José-Ramon Franco, Pascal Grébaut, Epco Hasker, Hamidou Ilboudo, Vincent Jamonneau, Mathurin Koffi, Veerle Lejon, Annette MacLeod, Justin Masumu, Enock Matovu, Raffaele Mattioli, Harry Noyes, Albert Picado, Kat S. Rock, Brice Rotureau, Gustave Simo, Sophie Thévenon, Sandra Trindade, Philippe Truc, Nick Van Reet,
Tópico(s)Neuroscience of respiration and sleep
Resumogambiense-HAT is targeted for elimination with zero transmission in humans. Innovative tools may contribute to the achievement of elimination; these tools include rapid diagnostic tests, improved tsetse-control tools, and an oral drug to treat both stages of disease. Research is revealing associations between infection outcome, including self-cure, and mutations within genes involved in immune responses. Patient-derived T. b. gambiense strains can cycle in animals and tsetse flies without losing infectivity to humans. Molecular and serological techniques facilitate new studies on naturally infected animals as putative reservoir hosts. Mathematical modelling supports the hypothesis that human or animal reservoirs drive transmission, and they, or the tsetse vectors, could be targeted to swiftly impact transmission. Ongoing modelling will assess possible recrudescence via reservoirs. Trypanosoma brucei gambiense causes human African trypanosomiasis (HAT). Between 1990 and 2015, almost 440 000 cases were reported. Large-scale screening of populations at risk, drug donations, and efforts by national and international stakeholders have brought the epidemic under control with <2200 cases in 2016. The World Health Organization (WHO) has set the goals of gambiense-HAT elimination as a public health problem for 2020, and of interruption of transmission to humans for 2030. Latent human infections and possible animal reservoirs may challenge these goals. It remains largely unknown whether, and to what extend, they have an impact on gambiense-HAT transmission. We argue that a better understanding of the contribution of human and putative animal reservoirs to gambiense-HAT epidemiology is mandatory to inform elimination strategies. Trypanosoma brucei gambiense causes human African trypanosomiasis (HAT). Between 1990 and 2015, almost 440 000 cases were reported. Large-scale screening of populations at risk, drug donations, and efforts by national and international stakeholders have brought the epidemic under control with <2200 cases in 2016. The World Health Organization (WHO) has set the goals of gambiense-HAT elimination as a public health problem for 2020, and of interruption of transmission to humans for 2030. Latent human infections and possible animal reservoirs may challenge these goals. It remains largely unknown whether, and to what extend, they have an impact on gambiense-HAT transmission. We argue that a better understanding of the contribution of human and putative animal reservoirs to gambiense-HAT epidemiology is mandatory to inform elimination strategies. HAT is caused by two closely related parasites that are transmitted by tsetse flies. Trypanosoma brucei gambiense is responsible for the Western and Central African form of the disease and Trypanosoma brucei rhodesiense occurs in Eastern and Southern Africa – both forms of the disease are usually fatal if untreated [1Büscher P. et al.Human African trypanosomiasis.Lancet. 2017; 390: 2397-2409Abstract Full Text Full Text PDF PubMed Scopus (370) Google Scholar]. Between 1990 and 2016, a total of 437 971 cases of gambiense-HAT were reported, with a peak of 37 385 cases in 1998i. Thanks to large-scale deployment of a serological screening test (CATT/T. b. gambiense) (see Glossary), drug donations, and intense efforts by national and international stakeholders, this epidemic has been brought under control, with fewer than 2200 cases reported in 2016. This represents a marked reduction in human suffering caused by the disease. Inspired by this progress, the WHO has set elimination of gambiense-HAT as a target for the near future: elimination as a public health problem by 2020 and the interruption of transmission to humans by 2030ii. The rationale to shift from HAT control to elimination is based on several arguments, such as the epidemiological vulnerability of gambiense-HAT as a presumed anthroponotic infection, historic examples of elimination in several West African foci, the availability of new medicines and diagnostics, the political will of endemic countries, and the commitment of national control programs [2World Health Organization Control and surveillance of human African trypanosomiasis.WHO Tech. Rep. Series. 2013; 984: 1-237Google Scholar]. Furthermore, a drug donation agreement between pharmaceutical companies and WHO has made treatment freely available to endemic countries. gambiense-HAT control classically relies on three pillars: vector control, case finding, and treatment. HAT is a vector-borne disease, and the reduction of human–fly contact below a critical threshold would lead to zero transmission. Although vector control is critical to achieve the elimination/eradication goals, in practice, it will be hard to sustain control of all tsetse fly populations in all endemic countries. Vector control being only part of the solution, gambiense-HAT control will continue to rely to a great extent on surveillance, diagnosis, and treatment, both for reducing transmission and for monitoring progress towards these goals. The introduction of individual rapid diagnostic tests (RDTs) for gambiense-HAT may increase serological screening coverage as they can be performed in remote dispensaries devoid of technical facilities. Thus, they facilitate the integration of passive screening in the health system and play a role in a sustainable surveillance system. However, RDTs also have limitations – like CATT/T. b. gambiense, they only detect antibodies, and their specificity is not 100% [3Jamonneau V. et al.Accuracy of individual rapid tests for serodiagnosis of gambiense sleeping sickness in West Africa.PLoS Negl. Trop. Dis. 2015; 9e0003480Crossref PubMed Scopus (32) Google Scholar]. As a consequence, given the adverse effects and logistic constraints of current treatment, individuals who test positive in an RDT or in CATT must undergo microscopic examination of blood or lymph node fluid to confirm the presence of the parasite, followed by a lumbar puncture for stage determination, as different drugs are required to treat early- and late-stage disease [2World Health Organization Control and surveillance of human African trypanosomiasis.WHO Tech. Rep. Series. 2013; 984: 1-237Google Scholar]. In recent years, the highly toxic melarsoprol regimen, used to treat late-stage disease, has been replaced by a safer, though still rather complex, treatment requiring parenteral administration and hospitalisation. An oral treatment might become available in late 2018, and a single-dose treatment is entering phase III clinical trialsiii [4Mesu V.K.B.K. et al.Oral fexinidazole for late-stage African Trypanosoma brucei gambiense trypanosomiasis: a pivotal multicentre, randomised, non-inferiority trial.Lancet. 2017; (Published online November 4, 2017)https://doi.org/10.1016/S0140-6736(17)32758-7Abstract Full Text Full Text PDF PubMed Scopus (156) Google Scholar]. Whereas HAT elimination by 2020, as a public health problem, seems within reach, the sustained global elimination of HAT appears more challenging. Indeed, as long as the knowledge gaps surrounding the reservoir of T. b. gambiense in interepidemic periods are not filled, the concept of eradication of gambiense-HAT cannot be considered. We present the current research evidence about potential human and animal T. b. gambiense reservoirs and discuss their importance in the light of the gambiense-HAT elimination goals. Mathematical models show that the sustained transmission of HAT can be explained if a fraction of the HAT cases is systematically missed by the screening operations [5Rock K.S. et al.Quantitative evaluation of the strategy to eliminate human African trypanosomiasis in the Democratic Republic of Congo.Parasit. Vectors. 2015; 8: 532Crossref PubMed Scopus (58) Google Scholar]. Unfortunately, this is the case in many settings as a number of T. b. gambiense infections remain undiagnosed for several reasons [6Robays J. et al.The effectiveness of active population screening and treatment from sleeping sickness control in the Democratic republic of Congo.Trop. Med. Int. Health. 2004; 9: 542-550Crossref PubMed Scopus (85) Google Scholar]. First, not all infected people are reached by screening activities. Second, current diagnostic techniques do not pick up all T. b. gambiense infections due to lack of sensitivity of serological screening tests, of molecular techniques, or of the parasitological confirmation tests [7Mumba Ngoyi D. et al.Performance of parasitological and molecular techniques for the diagnosis and surveillance of gambiense sleeping sickness.PLoS Negl. Trop. Dis. 2014; 8e2954Crossref PubMed Scopus (25) Google Scholar]. These undiagnosed, yet infected, people will act as a human reservoir of the parasite and might sustain transmission, forming a maintenance population [8Viana M. et al.Assembling evidence for identifying reservoirs of infection.Trends Ecol. Evol. 2014; 29: 270-279Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar]. Still another potential category of human reservoir may consist of latent infections, also called 'healthy carriers', who do not always progress to clinical disease, though the relative contribution of these individuals to parasite transmission still needs to be documented (Box 1). These latently infected people may carry trypanosomes for years or even decades, as was first described half a century ago in West Africa, and later in patients refusing treatment in Côte d'Ivoire [9Jamonneau V. et al.Untreated infections by Trypanosoma brucei gambiense are not 100% fatal.PLoS Negl. Trop. 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Whether latently infected persons transmit the parasite sexually [12Rocha G. et al.Possible cases of sexual and congenital transmission of sleeping sickness.Lancet. 2004; 363: 247Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar], and whether sexual and congenital transmission plays a significant role in the epidemiology of gambiense-HAT [13Welburn S.C. et al.Beyond tsetse – Implications for research and control of human African trypanosomiasis epidemics.Trends Parasitol. 2016; 32: 230-241Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar], remains hypothetical. In Guinea, asymptomatic or latent infections were found to have consistently high titres in CATT/T. b. gambiense and to be positive in the immune trypanolysis test, although no parasites could be detected in blood or lymph node fluid during a 2-year follow-up period [14Ilboudo H. et al.Diversity of response to Trypanosoma brucei gambiense infections in the Forecariah mangrove focus (Guinea): perspectives for a better control of sleeping sickness.Microbes Infect. 2011; 13: 943-952Crossref PubMed Scopus (32) Google Scholar]. This observation is in line with the fact that trypanosomes can survive in the extravascular spaces of diverse organs such as the heart, the central nervous system, and the skin [15Kristensson K. Bentivoglio M. et al.Pathology of African trypanosomiasis.in: Dumas M. Progress in Human African Trypanosomiasis, Sleeping Sickness. Springer, 1999: 157-181Crossref Google Scholar, 16Blum J.A. et al.Cardiac involvement in African and American trypanosomiasis.Lancet Infect. 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Microsatellite profiles and genomic sequencing of parasites from latent infections and from clinical HAT patients are indistinguishable, suggesting that the latent infection phenotype is determined primarily by the host rather than by the parasite [24Kabore J. et al.Population genetic structure of Guinea Trypanosoma brucei gambiense isolates according to host factors.Infect. Genet. Evol. 2011; 11: 1129-1135Crossref PubMed Scopus (11) Google Scholar]. Studies on host genetic polymorphism show that tumor necrosis factor-α-308 A, HLA-G UTR-2, APOL1 N264K, and APOL1 G2 are associated with increased risk of infection or with disease progression, while IL10-592 A, IL64339, APOL1 G1, and other polymorphisms in HPR and APOL1 are associated with decreased risk of infection or with latent infection [25Courtin D. et al.Association between human African trypanosomiasis and the IL6 gene in a Congolese population.Infect. Genet. 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Other studies have found associations between the innate and the adaptive immune response and infection outcome, for example, self-cure and high levels of interleukin-8 (IL-8); latent infection and high levels of IL-6 or specific interferon-γ-producing T cells; disease progression and high levels of IL-10, TNF-α, and sHLA-G [31Ilboudo H. et al.Trypanosome-induced Interferon-gamma production in whole blood stimulation assays is associated with latent Trypanosoma brucei gambiense infections.Microbes Infect. 2016; 18: 436-440Crossref PubMed Scopus (8) Google Scholar, 32Ilboudo H. et al.Unravelling human trypanotolerance: IL8 is associated with infection control whereas IL10 and TNFalpha are associated with subsequent disease development.PLoS Pathog. 2014; 10e1004469Crossref PubMed Scopus (30) Google Scholar, 33Gineau L. et al.Human Leukocyte Antigen-G: a promising prognostic marker of disease progression to improve the control of human African trypanosomiasis.Clin. Infect. Dis. 2016; 63: 1189-1197PubMed Google Scholar]. In view of the global elimination of HAT, it is of the utmost importance to clarify the extent to which these human reservoirs contribute to the transmission of the parasite and hence to gambiense-HAT persistence and potential resurgence.Box 1Diversity in Outcomes of Human Trypanosoma brucei gambiense InfectionsThere is growing evidence that infection with T. b. gambiense does not always follow the classical course of the disease, that is, a first haemolymphatic stage followed by a second stage with central nervous system involvement progressing to death if left untreated (Figure I). These symptomatic HAT patients are characterised by the detection of parasites in any body fluid (P+), detection of specific antibodies against T. b. gambiense Variable Antigen Type LiTat 1.3 or LiTat 1.5 in immune trypanolysis (TL+), and the presence of clinical symptoms. However, long-term follow-up studies in West Africa have shown that a number of infected individuals do not develop the disease and can be classified as having latent infections (i.e., they are healthy carriers) [9Jamonneau V. et al.Untreated infections by Trypanosoma brucei gambiense are not 100% fatal.PLoS Negl. Trop. Dis. 2012; 6e1691Crossref PubMed Scopus (128) Google Scholar]. They remain asymptomatic without detectable parasites (P−) for several years, although they are consistently positive in the immune trypanolysis test (TL+). Moreover, some of them may become immune trypanolysis-negative (TL−) over time, suggesting that they self-cured and therefore cannot transmit the parasite any more. There is growing evidence that infection with T. b. gambiense does not always follow the classical course of the disease, that is, a first haemolymphatic stage followed by a second stage with central nervous system involvement progressing to death if left untreated (Figure I). These symptomatic HAT patients are characterised by the detection of parasites in any body fluid (P+), detection of specific antibodies against T. b. gambiense Variable Antigen Type LiTat 1.3 or LiTat 1.5 in immune trypanolysis (TL+), and the presence of clinical symptoms. However, long-term follow-up studies in West Africa have shown that a number of infected individuals do not develop the disease and can be classified as having latent infections (i.e., they are healthy carriers) [9Jamonneau V. et al.Untreated infections by Trypanosoma brucei gambiense are not 100% fatal.PLoS Negl. Trop. Dis. 2012; 6e1691Crossref PubMed Scopus (128) Google Scholar]. They remain asymptomatic without detectable parasites (P−) for several years, although they are consistently positive in the immune trypanolysis test (TL+). Moreover, some of them may become immune trypanolysis-negative (TL−) over time, suggesting that they self-cured and therefore cannot transmit the parasite any more. Compared to latent infections in humans, our current knowledge of T. b. gambiense infections in animals is very limited and fragmented. The presence of T. b. gambiense in animals has been demonstrated in several studies (Figure 1) [34Cecchi G. et al.Assembling a geospatial database of tsetse-transmitted animal trypanosomosis for Africa.Parasit. Vectors. 2014; 7: 39Crossref PubMed Scopus (53) Google Scholar, 35Cecchi G. et al.Developing a continental atlas of the distribution and trypanosomal infection of tsetse flies (Glossina species).Parasit. Vectors. 2015; 8: 284Crossref PubMed Scopus (44) Google Scholar]. Several authors have suggested that animals can act as a reservoir for gambiense-HAT [36Yesufu H.M. Experimental transmission of Trypanosoma gambiense in domestic animals.Ann. Trop. Med. Parasitol. 1971; 65: 341-347Crossref PubMed Scopus (8) Google Scholar, 37Molyneux D.H. Animal reservoirs and Gambian trypanosomiasis.Ann. Soc. Belg. Med. 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Evol. 2006; 6: 147-153Crossref PubMed Scopus (110) Google Scholar, 43Cordon-Obras C. et al.Molecular evidence of a Trypanosoma brucei gambiense sylvatic cycle in the human african trypanosomiasis foci of Equatorial Guinea.Front. Microbiol. 2015; 6: 765Crossref PubMed Scopus (16) Google Scholar, 44Mehlitz D. The behaviour in the blood incubation infectivity test of four Trypanozoon strains isolated from pigs in Liberia.Trans. R. Soc. Trop. Med. Hyg. 1977; 71: 86Abstract Full Text PDF PubMed Scopus (16) Google Scholar, 45N'Djetchi M.K. et al.The study of trypanosome species circulating in domestic animals in two human African trypanosomiasis foci in Côte d'Ivoire identifies pigs and cattle as potential reservoirs of Trypanosoma brucei gambiense.PLoS Negl. Trop. Dis. 2017; 11e0005993PubMed Google Scholar]. In rhodesiense-HAT, sustained parasite transmission cycles exist in both livestock and wildlife, from which the parasite can spill over to humans [46Simarro P.P. et al.The atlas of human African trypanosomiasis: a contribution to global mapping of neglected tropical diseases.Int. J. Health Geogr. 2010; 9: 57Crossref PubMed Scopus (260) Google Scholar]. For T. b. gambiense, despite early data generated on its infectivity and transmissibility in animals, the epidemiological significance of any animal reservoir is not well understood and may depend on the specific ecosystem of the HAT focus. Even if the parasite can be transmitted to and from animals, factors such as the proportion of blood-feeding on that species by tsetse will determine the epidemiological significance of the species to act as a maintenance population or part of a maintenance community. T. b. gambiense can infect a variety of domestic animals and wildlife, as shown in Table 1. Following infection, most of these animals remain asymptomatic and generally show low to very low parasitaemia. For instance, in pigs infected with a T. b. gambiense strain isolated from a human patient, only xenodiagnosis and blood culture succeeded in revealing an infection but conventional microscopy failed to detect parasites [47Van Hoof L. et al.Recherche sur le comportement de Trypanosoma gambiense chez le porc.Ann. Soc. Belg. Med. Trop. 1940; 20: 203-228Google Scholar, 48Van Hoof L.M.J.J. Observations on trypanosomiasis in the Belgian Congo.Trans. R. Soc. Trop. Med. Hyg. 1947; 40: 728-761PubMed Google Scholar, 49Corson J.F. A third note on a strain of Trypanosoma gambiense transmitted by Glossina morsitans.Ann. Trop. Med. Parasitol. 1938; 32: 245-248Crossref Scopus (1) Google Scholar, 50Duke N.L. Antelope and their relation to trypanosomiasis.Proc. R. Soc. Lond. B. 1913; 85: 156-169Crossref Google Scholar, 51Wombou Toukam C.M. et al.Experimental evaluation of xenodiagnosis to detect trypanosomes at low parasitaemia levels in infected hosts.Parasite. 2011; 18: 295-302Crossref PubMed Scopus (20) Google Scholar]. Moreover, experimental studies have shown that human-derived T. b. gambiense strains that were cyclically transmitted by tsetse flies between animals for more than a year remained transmissible to humans [48Van Hoof L.M.J.J. Observations on trypanosomiasis in the Belgian Congo.Trans. R. Soc. Trop. Med. Hyg. 1947; 40: 728-761PubMed Google Scholar].Table 1Animals Successfully Infected with T. b. gambiense Strains Isolated from Human PatientsAnimal speciesOrigin of trypanosome strainaFor reasons of traceability, we use the name of countries and the scientific name of animals as mentioned in the original publication: Senegambia=Senegal and The Gambia; Belgian Congo, Congo Free State and Congo Belge=Democratic Republic of the Congo; République populaire du Congo=Republic of the Congo.Infectiveness to tsetseMinimum observed duration of infectionRefsDomestic animalsCatSenegambia and Congo Free StateNot tested12 days73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google ScholarCattleNigeriaYes50 days66Joshua R.A. et al.Isolation of human serum resistant Trypanozoon from cattle in Nigeria.Tropenmed. Parasitol. 1983; 34: 201-202PubMed Google Scholar, 74Moloo S.K. et al.Cyclical development of Trypanosoma brucei gambiense from cattle and goats in Glossina.Acta Trop. 1986; 43: 407-408PubMed Google ScholarChickenUnknownNot tested75 days75Mesnil F. Blanchard M. Infections des poules dues aux Trypanosoma gambiense et Tryp rhodesiense.C. R. Soc. Biol. 1912; 72: 938-940Google ScholarDogSenegambia and Congo Free State, Nigeria; Belgian CongoYes109 days36Yesufu H.M. Experimental transmission of Trypanosoma gambiense in domestic animals.Ann. Trop. Med. Parasitol. 1971; 65: 341-347Crossref PubMed Scopus (8) Google Scholar, 48Van Hoof L.M.J.J. Observations on trypanosomiasis in the Belgian Congo.Trans. R. Soc. Trop. Med. Hyg. 1947; 40: 728-761PubMed Google Scholar, 73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google ScholarDonkeySenegambiaNot tested14 days73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google ScholarGoatSenegambia, Nigeria, Belgian CongoYes13 months48Van Hoof L.M.J.J. Observations on trypanosomiasis in the Belgian Congo.Trans. R. Soc. Trop. Med. Hyg. 1947; 40: 728-761PubMed Google Scholar, 73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google Scholar, 74Moloo S.K. et al.Cyclical development of Trypanosoma brucei gambiense from cattle and goats in Glossina.Acta Trop. 1986; 43: 407-408PubMed Google ScholarHorseSenegambiaNot tested5 months73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google ScholarPigCôte d'Ivoire, Congo Belge, NigeriaYes18 months47Van Hoof L. et al.Recherche sur le comportement de Trypanosoma gambiense chez le porc.Ann. Soc. Belg. Med. Trop. 1940; 20: 203-228Google Scholar, 51Wombou Toukam C.M. et al.Experimental evaluation of xenodiagnosis to detect trypanosomes at low parasitaemia levels in infected hosts.Parasite. 2011; 18: 295-302Crossref PubMed Scopus (20) Google Scholar, 76Watson, H.J.C. (1962). The domestic pig as a reservoir of T. gambiense In 9th Meeting of the International Scientific Council for Trypanosomiasis Research and Control, Conakry, Guinea (Commission de Coopération Technique en Afrique au Sud du Sahara, ed), p. 327Google ScholarSheepCôte d'IvoireNot tested77Bouteille B. et al.Experimental models for new chemotherapeutic approaches to human African trypanosomiasis.in: Dumas M. Progress in Human African Trypanosomiasis, Sleeping Sickness. Springer, 1999: 289-300Crossref Google ScholarPrimatesAgile mangabey (Cercocebus galeritus agilis)Belgian CongoYes48Van Hoof L.M.J.J. Observations on trypanosomiasis in the Belgian Congo.Trans. R. Soc. Trop. Med. Hyg. 1947; 40: 728-761PubMed Google ScholarGreen monkey (Cercopithecus callitrichus, C. aethiops tantalus)Congo Free State, NigeriaYes3 months36Yesufu H.M. Experimental transmission of Trypanosoma gambiense in domestic animals.Ann. Trop. Med. Parasitol. 1971; 65: 341-347Crossref PubMed Scopus (8) Google Scholar, 73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping sickness with those of Trypanosoma gambiense (Dutton).Lancet. 1904; : 1337-1340Google ScholarWolf's mona monkey (Cercopithecus wolfi)Congo BelgeYes15 days47Van Hoof L. et al.Recherche sur le comportement de Trypanosoma gambiense chez le porc.Ann. Soc. Belg. Med. Trop. 1940; 20: 203-228Google ScholarPatas monkey (Erythrocebus patas patas)NigeriaYes3 months36Yesufu H.M. Experimental transmission of Trypanosoma gambiense in domestic animals.Ann. Trop. Med. Parasitol. 1971; 65: 341-347Crossref PubMed Scopus (8) Google Scholar, 78Godfrey D.G. Killick-Kendrick R. Cyclically transmitted infections of Trypanosoma brucei, T: rhodesiense and T. gambiense in chimpanzees.Trans. R. Soc. Trop. Med. Hyg. 1967; 61: 781-791Abstract Full Text PDF PubMed Scopus (22) Google ScholarRhesus macaque (Macacus rhesus)Senegambia and Congo Free StateNot tested1 month73Thomas H.W. Linton S.F. A comparison of the animal reactions of the trypanosomes of Uganda and Congo Free State sleeping si
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